Invasive crayfish depress dragonflies and boost mosquitoes

June 9, 2019 by fredsingerecology

Paradoxically, obliviousness and intense focus can be two sides of the same coin, as the following story highlights. As a new graduate student at the University of Minnesota, I took a field ecology course at the University’s field station at Lake Itasca (famously known as headwaters of the Mississippi River). One afternoon we watched dragonflies at a small pond; the male dragonflies were obviously patrolling territories and behaving thuggishly whenever intruders came by, and amorously whenever females of their species approached. Surprisingly, territorial males chased off male intruders of any species, even though they posed no reproductive threat to them. Why, I wondered… So I sat there for many hours and kept very careful track of who chased whom, and for how long. Big focus time. Ultimately, these observations blossomed into my doctoral dissertation. Unfortunately, these observations also blossomed into the most virulent case of poison ivy known to humanity, as my intense focus on dragonflies obliviousized me to the luxurious patch of poison ivy, which served as my observation perch.

Anax junius dragonflies in copula. The male has the bright blue abdomen. Credit: Henry Hartley.

Despite this ignoble incident, dragonflies remain one of my favorite animal groups. They are strikingly beautiful, brilliant flyers, and fun to try to catch. In addition, they have so many wonderful adaptations, including males with penises that are shaped to scoop out sperm (previously introduced by another male) from their mate’s spermatheca, and females who go to extremes to avoid repeated copulation attempts, for example, by playing dead when approached by a male. Thus I was delighted to come across research by Gary Bucciarelli and his colleagues that highlighted the important role dragonflies play in stream ecosystems just west of Los Angeles, California.

Captured dragonfly nymph. Dragonflies require from one to four years to develop in aquatic systems, before they metamorphose into terrestrial winged adults. As nymphs, they are fearsome predators on aquatic invertebrates. As adults, they specialize on winged insects, though there are stories of them killing small birds. Credit: Gary Bucciarelli

Bucciarelli and his colleagues came up with their research question as a result of working in local streams with students on a different project. They wanted to know if invasive non-native crayfish (Procambarus clarkii) affect the composition of stream invertebrates and whether removal of crayfish could lead to rapid recovery of these invertebrate communities.

Invasive crayfish, P. clarkii, sits on the stream bottom. Credit: Gary Bucciarelli

The researchers collected stream invertebrate samples and noticed a dramatic pattern – in all the streams with crayfish there were numerous mosquito larvae, but in all of the streams without crayfish there were no mosquito larvae and much greater numbers of dragonfly nymphs. This led them to formulate and test two related hypotheses. First, dragonfly nymphs (Aeshnaspecies) are more efficient predators on mosquitoes (Anopheles species) than are the invasive crayfish. Second, crayfish interfere with dragonfly predation on mosquitoes in streams where crayfish and dragonflies are both present.

Student researchers collect stream samples. Credit: Gary Bucciarelli

Bucciarelli and his colleagues systematically sampled 13 streams monthly from March to October 2016 in the Santa Monica Mountains. Eight streams have had crayfish populations since the 1960s, while four streams never had crayfish, and one stream had crayfish removed as part of a restoration effort in 2015. Overall, streams with crayfish had a much lower number of dragonfly nymphs than did streams without crayfish. In addition, streams with crayfish had substantial populations of Anopheles mosquitoes, while streams without crayfish (but much higher dragonfly populations) had no Anopheles mosquitoes in the samples.

Number of mosquito larvae (MSQ) and dragonfly nymphs (DF) by month in streams with crayfish (CF – top row of data) or without crayfish (CF Absent – bottom row)

This field finding supports both of the hypotheses, but the evidence is purely correlational. So the researchers brought the animals into the laboratory to test predation under more controlled conditions. They introduced 15 mosquito larvae into tanks, and exposed them to one of four treatments: (1) a single crayfish, (2) a single dragonfly nymph, (3) one crayfish and one dragonfly nymph, or (4) no predators. The researchers counted the numbers of survivors periodically over the three day trials. As the graph below indicates, dragonflies are vastly superior consumers of mosquito larvae compared to crayfish. However, when forced to share a tank with crayfish, dragonflies stop hunting, either huddling in corners or actually perching on the crayfish. By 36 hours into the experiment, all of the dragonflies had been eaten by the crayfish. After three days, mosquito survival was similar when comparing tanks with crayfish alone with tanks that had both a crayfish and a dragonfly.

Mean number of surviving mosquito larvae in tanks with a lone dragonfly (DF), a lone crayfish (CF), one crayfish and one dragonfly (CF+DF) in comparison to controls with no predators.

Bucciarelli and his colleagues conclude that dragonfly nymphs are much more efficient predators of mosquito larvae than are crayfish. But when placed together with crayfish, dragonfly foraging efficiency plummeted. Field surveys showed a negative correlation between crayfish abundance and dragonfly larvae, and much greater mosquito larva populations in streams with crayfish. This supports the conclusion that invasive crayfish cause mosquito populations to increase sharply by depressing dragonfly populations and foraging efficiency. This is a complex trophic cascade because crayfish increase mosquito populations despite eating a substantial number of mosquito individuals.

The researchers argue that crayfish probably relegate dragonfly larvae to inferior foraging habitats, thereby limiting their efficiency as mosquito predators. As such, ecosystem services provided by dragonflies to humans are greatly diminished. Recently, several new mosquito species that are disease vectors have moved into California. Thus the loss of dragonfly predation services could pose a public health threat to the human population. Bucciarelli and his colleagues recommend removing the invasive crayfish to restore the natural community of predators, including dragonflies, which will then naturally regulate the increased number of potential disease vectors.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Bucciarelli, G. M., Suh, D. , Lamb, A. D., Roberts, D. , Sharpton, D. , Shaffer, H. B., Fisher, R. N. and Kats, L. B. (2019), Assessing effects of non‐native crayfish on mosquito survival. Conservation Biology, 33: 122-131. doi:10.1111/cobi.13198. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Quoll vs. toad: a toxic brew

May 6, 2019 by fredsingerecology

A native of Central and South America, the cane toad, Rhinella marina, was introduced to Australia in 1935 with great fanfare. The plan was for the voracious cane toad to eat all of the grey-backed cane beetles that were plaguing sugar cane plantations in northern Australia (a similar introduction had been successful in Puerto Rico). But the plan failed, in part because there was no cover from predators, so the toads were not enthusiastic about hanging out in sugar cane plantations, and in part because adult beetles live primarily near the tops of sugar cane, and cane toads are poor climbers.

A cane toad. Credit: Ben Philips

So now, northern Australia has a cane toad plague, which is wreaking havoc on ecosystems, and threatening many native species, including the northern quoll, Dasyurus hallucatus. These omnivorous marsupials eat fruit, invertebrates and small vertebrates. Unfortunately, their long list of food items includes cane toads, which are highly toxic to most consumers, having poison glands that contain bufotoxin, a composite of several very nasty chemicals. If a northern quoll eats a cane toad, it’s bye bye quoll.

Male captive born northern quoll_EllaKelly

A northern quoll. Credit: Ella Kelly.

Unfortunately most quolls have not gotten the message; huge numbers are dying, and populations are going extinct. As toads continue their invasion from north to south, more quoll populations, particularly those in northwestern Australia, will be at risk.

Map of Australia showing past (light shading) and recent (dark shading) northern quoll distribution, and present (solid line) and future (dashed line) cane toad distribution.

Some quolls show “toad-smart” behavior and don’t eat toads. Ella Kelly and Ben Phillips are trying to understand how this happens. This is particularly important because a few quoll populations have managed to survive the cane toad plague by virtue of being toad-smart (though 95% of quoll populations have gone extinct in the wake of the cane toad wave). The researchers reason that if there is a genetic basis to toad-smart behavior, it might be possible to introduce toad-smart individuals into populations that have not yet been overrun by cane toads. These individuals with toad-smart genes would breed and spread their genes through their adopted population. This strategy of targeted gene flow would give the recipient population the genetic variation needed, so that some individuals (those with toad-smart genes) would be more likely to survive the cane toad invasion. Over time toad-smart behavior would spread throughout the population via natural selection.

Targeted gene flow requires the trait to be influenced by genes. To test for a genetic basis to the toad-smart trait, Kelly and Phillips designed a common-garden experiment, capturing some quolls that had survived the cane toad invasion (toad-exposed), and others from regions that had not yet been exposed (toad-naïve). At Territory Wildlife Park, Northern Territory, Australia, the researchers bred these quolls to create three lines of offspring: Toad-exposed x toad-exposed, toad-exposed x toad-naïve (hybrids), and toad-naïve x toad-naïve. They raised these three lines under identical conditions at the park. Kelly and Phillips then asked, are there behavioral differences in how these three lines respond to cane toads?

Northern quoll captured in Northern Territory, Australia. Credit: Ella Kelly.

The researchers set up two experiments. First they asked, which would a quoll (that had never before experienced a cane toad) prefer to investigate if given the choice: a dead cane toad or a dead mouse? It turned out that the quoll offspring with two toad-exposed parents were somewhat more interested in mice than in cane toads. The same was true for the hybrids. However, the toads with two toad-naïve parents showed little preference.

Second, and more important, the researchers gave quolls from the three lines the opportunity to eat a toad leg (which does not have enough poison to harm the quoll). The results of this experiment were striking; offspring of toad-naïve parents were twice as likely to eat the toad leg than were offspring of toad-exposed parents, or hybrids with one parent of each type.

Proportion of toad-naive (both parents toad-naive), hybrid and toad-exposed (both parents toad-exposed) quoll offspring that ate a cane toad leg. Error bar = +/- 1 SE.

Kelly and Phillips conclude that toad-smart behavior is a genetically-based trait that has been under strong natural selection in populations of quolls that survived the cane toad invasion. Hybrid offspring behave similarly to the offspring of two toad-exposed parents, suggesting that toad-smart behavior has a dominance inheritance pattern. The researchers propose using targeted gene flow, in this case introducing toad-adapted individuals into populations prior to the arrival of cane toads. Recently, Kelly and Phillips released 54 offspring with toad-smart genetic backgrounds onto Indian Island, which is about 40 km from Darwin. The island has a large cane toad population, so the researchers will follow the introduced quoll population to see whether it is genetically equipped to survive in the presence of the cane toad scourge.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kelly, E. and Phillips, B. L. (2019), Targeted gene flow and rapid adaptation in an endangered marsupial. Conservation Biology, 33: 112-121. doi:10.1111/cobi.13149. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Invasive engineers alter ecosystems

April 25, 2019 by fredsingerecology

Ecosystem engineers change the environment in a way that influences the availability of essential resources to organisms living within that environment. Beavers are classic ecosystem engineers; they chop down trees and build dams that change water flow and provide habitat for many species, and alter nutrient and food availability within an ecosystem. Ecologists are particularly interested in understanding what happens when an invasive species also happens to be an ecosystem engineer; how are the many interactions between species influenced by the presence of a novel ecosystem engineer?

For her Ph.D research Linsey Haram studied the effects of the invasive red alga Gracilaria vermiculophylla on native estuarine food webs in the Southeast USA. She wanted to know how much biomass this ecosystem engineer contributed to the system, how it decomposed, and what marine invertebrates ate it. She was spending quite a lot of time in Georgia’s knee-deep mud at low tide, and became acquainted with the shorebirds that zipped around her as she worked. She knew that small marine invertebrates are attracted to the seaweed and are abundant on algae-colonized mudflats, and she wondered if the shorebirds were cueing into that. If so, the non-native alga could affect the food web both directly, by providing more food to invertebrate grazers, and indirectly, by providing habitat for marine invertebrates and thus boosting resources for shorebirds.

A least sandpiper forages on a red algae-colonized mudflat. Credit: Linsey Haram.

Since the early 2000’s, Gracilaria vermiculophylla has dramatically changed estuaries in southeast USA by creating novel habitat on mudflats that had previously been mostly bare, due to high turbidity and a lack of hard surface for algal attachment. But this red alga has a symbiotic association with a native tubeworm, Diopatra cuprea, that attaches the seaweed to its tube so it can colonize the mudflats. This creates a more hospitable environment to many different invertebrates, providing cover from heat, drying out, and predators, while also providing food to invertebrates that graze on the algae.

Closeup view of the red alga Gracilaria vermiculophylla, an invasive ecosystem engineer. Credit: Linsey Haram

Haram and her colleagues decided to investigate how algae presence might be influencing bird distribution and behavior. They realized that this influence might be scale-dependent; on a large spatial scale birds may see the algae from afar and be drawn to an algae-rich mudflat, while on a smaller spatial scale, differences in foraging behavior may lead to differences in how a particular species uses the algal patches in comparison to bare patches.

To explore large scale effects, the researchers counted all shorebirds (as viewed from a boat) on 500 meter transects along six bare mudflats and six algal mudflats. They also measured algal density (even algal mudflats have large patches without algae), and invertebrate distribution and abundance both on the surface and buried within the sediment. These surveys showed that shorebirds, in general, were much more common on algal mudflats. As you can see, this trend was stronger in some shorebird species than others, and one species (graph f below) showed no significant trend.

Field surveys of shorebird density (#/ha) on six bare mudflats compared to six mudflats colonized by Gracilaria vermiculophylla. * indicates weak trend (0.05 < P < 0.10), ** indicates a stronger difference (P < 0.05). Bold horizontal bars are median values. Common names of species are (b) dunlin, (c) small sandpipers, (d) ruddy turnstone, (e) black-bellied plover, (f) semipalmated plover, (g) willet, (h) short-billed dowitcher.

Algal mudflats had a much greater abundance and biomass of invertebrates living on the surface, particularly isopods and snails, which presumably attracted some of these birds. However, below the surface, there were no significant differences in invertebrate abundance and biomass when comparing mudflats with and without algae.

Having shown that on a large spatial scale shorebirds tend to visit algal mudflats, Haram and her colleagues then turned their attention to bird preferences on a smaller spatial scale. First, they conducted experiments on an intermediate scale, observing bird foraging preferences on 10 X 20 plots with or without algae. They then turned their attention to an even smaller scale, by observing the foraging behavior on a <1m²scale. On each sampling day, the researchers observed individuals of seven different shorebird species on a mudflat with algal patches, to see whether focal birds spent more time foraging on algal patches or bare mud. During each 3-minute observation, researchers recorded the number of pecks made into algal patches vs. bare mud, and compared that to the expected peck distribution based on the observed ratio of algal-cover to bare mud (which was a ratio of 27:73).

On the smallest scale, two of the species, Calidras minutilla and Aranaria interpres, showed a very strong preferences for foraging in algae, while a third species, Calidris alpine, showed a weak algal preference. In contrast, Calidris species (several species of difficult-to-distinguish sandpipers) and Charadrius semipalmatus strongly preferred foraging in bare mud, while the remaining two species showed no preference.

Small-scale foraging preferences (x–axis) of shorebirds. Solid blue curve is the strength of population preference (in terms of probability – y-axis) for mudflats, while solid red curve is the strength of population preference for algae. Dashed curves are individual preferences. Red arrows at 0.27 indicates the proportion of the mudflat that is covered with algae, while the blue arrow at 0.73 represents the proportion of bare mudflat (and hence indicate random foraging decisions). Filled arrows are significantly different from random, shaded arrows are slightly different from random, while unfilled arrows are random. Common names of species are: (a) dunlin, (b) least sandpiper, (c) small sandpipers, (d) ruddy turnstone, (e) semipalmated plover, (f) willet, (g) short-billed dowitcher.

If you compare the two sets of graphs above, you will note that in some cases shorebird preferences for algae are similar across large and small spatial scales, but for other species, these preferences may vary with spatial scale. For example, Arenaria interpres was attracted to algal mudflats on a large scale, and once present, these birds foraged exclusively amongst the algae, shunning any mud that lacked algae. Small sandpipers (Calidris species) also were attracted to algal mudflats on a large scale, but in contrast to Arenaria interpres, these sandpipers foraged exclusively in bare mud, rather than in the algae.

The researchers conclude that different species have different habitat preferences across spatial scales in response to Gracilaria vermiculophylla. Most, but not all, species were more attracted to mudflats that harbored the invasive ecosystem engineer. But once there, shorebird small-scale preference varied in response to species-specific foraging strategy. For example, the ruddy turnstone (Arenaria interpres) discussed in the previous paragraph, forages by turning over stones (hence its name) shells and clumps of vegetation, eating any invertebrates it uncovers. Accordingly, it forages primarily in algal clumps. In contrast, willets (Tringa semipalmata), short-billed dowitchers (Limnodromus griseus) and dunlins (Calidris alpine) were all attracted strongly to algal mudflats, but showed basically random foraging on a small spatial scale, showing little or no preference for algal clumps. The researchers explain that these three species use their very long beaks to probe deeply beneath the surface, using tactile cues to grab prey. So unlike the ruddy turnstone and some other species that forage for surface invertebrates, they don’t use the algae as a cue that food is available below. Thus species identity, and consequent morphology, behavior and foraging niche are all important parts of how a community responds to an invasive ecosystem engineer.

note: the paper that describes this research is from the journal Ecology. The reference is Haram, L. E., Kinney, K. A., Sotka, E. E. and Byers, J. E. (2018), Mixed effects of an introduced ecosystem engineer on the foraging behavior and habitat selection of predators. Ecology, 99: 2751-2762. doi:10.1002/ecy.2495. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

The complex life of the pea

April 15, 2019 by fredsingerecology

As a behavioral ecologist, I’m spending a surprising amount of time reading and writing about plants these days. It turns out that plants are amazingly complex and interactive; you just need to know where and how to look. Today we will discuss the humble pea plant, how it is infected with a virus that is carried by an aphid that sucks its xylem, and how a herbivorous weevil fits into the whole system. The virus is the pea enation mosaic virus (PEMV), which causes pea leaves to yellow and wither, and also creates enations (scaly tissue) to develop on a leaf’s undersides. The aphid vector (a vector is the organism that carries a disease) is Acrythosiphon pisum, while the herbivorous weevil is Sitona lineatus.

Pea plant infected with pea enation mosaic virus. Credit Paul Chisholm.

David Crowder has been studying plant/insect interactions for many years, and knew that most researchers who studied interactions between plants and insect vectors focused their attention on the plants, insects and the disease, but did not consider how other species in the community might affect this relationship. Paul Chisholm was a PhD student in Crowder’s lab; and working with two other researchers, they explored whether S. lineatus, an abundant herbivore of peas, influenced viral transmission. They expected that if the pea was first attacked by the weevil, it might be more susceptible to subsequent viral infection. Conversely, if the pea was infected by the virus, it might be less able to chemically defend itself against subsequent herbivory by the weevil.

(Left) Pea aphids. Credit: Shipher Wu under a Creative Commons Attribution 4.0 International Public License. (Right) Very adult pea leaf weevils, Sitona lineatus. Credit: Gail Hampshire under a Creative Commons Attribution 4.0 International Public License

It is easy to visually distinguish between PEMV-infected and uninfected plants, so the researchers could assess whether infected plants tended to suffer more defoliation by weevils than did uninfected plants. They visited 12 different fields in northern Washington and western Idaho, USA, and measured defoliation by counting the number of feeding notches left by the weevils after feeding on 3 – 10 infected pea plants and an equal number of nearby uninfected plants on each field (more feeding notches = more defoliation). They discovered that PEMV-infected plants tended to suffer substantially higher herbivory than did uninfected plants

Herbivory (as measured by number of feeding notches) caused by weevils on paired uninfected (black bars) and PEMV-infected (blue bars) pea plants sampled from 12 different fields. Error bars for all figures represent 1 SE.

Given the correlation between herbivory and infection, Chisholm and his colleagues then explored whether (1) the weevil preferred to feed on infected plants, and/or whether (2) infective aphids preferred to feed on plants that had been damaged by herbivorous weevils. Both questions were answered with behavioral choice assays done in a greenhouse. First, the researchers created two groups of pea plants. The first group, sham infected, were fed on by aphids not carrying PEMV for 48 hours, while the second group of plants were fed on by PEMV-infected aphids for the same duration. Aphids were removed and PEMV infection developed within 15 days in the PEMV infected plants. The researchers then set up one sham infected and one PEMV-infected plant in a test cage, and released two weevils equidistant from the plants, allowing them to feed for six days. They discovered that aphids fed much more voraciously on the PEMV-infected plants.

Mean leaf area removed from sham infected and PEMV-infected pea plants.

For the second experiment, the researchers again created two types of plants: undamaged – no herbivory, and damaged – 48 hours of weevil herbivory. Weevils were then removed, and one leaf from each plant was connected to each end of a tube, while still attached to each plant.

Experimental setup with tube attached to one leaf of each experimental plant. Aphids were introduced into the central tube. Credit Paul Chisholm.

The researchers added either 25 infectious or 25 non-infectious aphids, and allowed them 3 hours to choose a leaf. PEMV-infected aphids preferred damaged leaves, while uninfected aphids showed no preference.

PEMV-infected aphid preference for undamaged (no herbivory) or damaged (weevil herbivory) leaves.

Chisholm and his colleagues then turned their attention to whether weevil herbivory made pea plants more susceptible to PEMV infection. In one experiment they allowed PEMV-infected aphids to feed on plants for 3 days, and then introduced 0, 1 or 3 weevils who fed on the plants for another 6 days. They used a protein assay to estimate the PEMV-titer (concentration) of each plant and discovered that the plants that were exposed to greatest herbivory had the highest PEMV titer (see graph below). In a second experiment the researchers allowed weevil herbivory before adding the aphids, and found no effect of prior herbivory on PEMV titer.

Relative PEMV-titer of infected leaves after they were subjected to herbivory by zero, one or three weevils for six days. different letters above bars indicate significant differences between treatments.

What causes these plant responses to challenges by PEMV and weevils? The researchers discovered that levels of three important plant hormones increased either in response to PEMV infection, weevil herbivory or both. At this point it is not clear how these different hormone levels interact to bring about the changes we’ve described.

The researchers conclude that weevil behavior has a profound influence on the interactions between aphids, the viruses they carry and the pea plants they feed on (and infect). The weevil is not a vector for the virus, yet it affects the virus directly by altering plant behavior and physiology and indirectly by altering the behavior of the vector (the aphids). PEMV outbreaks are more likely when weevils are abundant, as aphids prefer damaged plants, and feeding by weevils increased the PEMV titer in infected plants. Crowder argues that interactions in which a non-vector species influences the relationship between a host and its vector (and the pathogen it carries) are probably extraordinarily common in crop systems. So if we want to understand crop susceptibility to pathogens we need to cast a broad net and consider both the direct and indirect effects of a community of species that can influence how the crop responds to infection.

note: the paper that describes this research is from the journal Ecology. The reference is Chisholm, P. J., Sertsuvalkul, N. , Casteel, C. L. and Crowder, D. W. (2018), Reciprocal plant‐mediated interactions between a virus and a non‐vector herbivore. Ecology, 99: 2139-2144. doi:10.1002/ecy.2449. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Beautiful buds beset bumblebees with bad bugs

February 28, 2019 by fredsingerecology

Sexual liaisons can be difficult to achieve without some type of purposeful motion. Flowering plants, which are rooted to the ground, are particularly challenged to bring the male close enough to the female to have sex. One awesome adaptation is pollen, technically the male gametophyte – or gamete (sperm)-generating plant. These tiny males get to females either by floating through the air, or by being transferred by animal pollinators such as bees. Plants can lure bees to their flowers by producing nectar – a sugar rich fluid – which bees lap up and use as a carbohydrate source. While nectaring, bees also collect pollen, either intentionally or inadvertently, which provides them with essential proteins. When bees travel to the next flower, they may inadvertently drop some of their pollen load near the female gametophyte – in this case a tiny egg-generating plant (though tiny, the female gametophyte is considerably larger than is the male gametophyte). We call this process of “tiny boy meets tiny girl” pollination. Once the two gametophytes meet, the pollen produces one or more sperm, which it uses to fertilize an egg within the female gametophyte. There is more to it, but this will hopefully clarify the difference between pollination and fertilization.

Bumblebee forages on beebalm, Monarda didyma. Credit: Jonathan Giacomini.

All of this business takes place within the friendly confines of the flower. The same flower may be visited by many different bees of many different species. While feeding, bees carry on other bodily functions, including defecation. They are not careful about where they defecate; consequently a bee’s breakfast might also include feces from a previous bee visitor. Bumblebee (Bombus impatiens) feces carries many disease organisms, including the gut parasite Crithidia bombi, which can reduce learning, decrease colony reproduction and impair a queen’s ability to found new colonies. Because pollinators are so critical in ecosystems, Lynn Adler and her colleagues wondered whether certain types of flowers were better vectors for harboring and transmitting Crithidia bombi to other bumblebees.

Bumblebee forages on the snapdragon, Antirrhinum majus. Credit: Jonathan Giacomini.

The researchers chose 14 different flowering plant species, allowing uninfected bumblebees to forage on inflorescences (clusters of flowers) inoculated with a measured amount of Crithidia bombi parasites. The bees were reared for seven days after exposure, and then were assessed for whether they had picked up the infection from their foraging experience, and if so, how intense the infection was. The researchers dissected each tested bee and counted the number of Crithidia cells within the gut.

Researcher conducts foraging trial with Lobelia siphilitica inflorescence. Credit: Jonathan Giacomini.

Adler and her colleagues discovered that some plant species caused a much higher pathogen count (mean number of infected cells in the bee gut) than did other plant species. For example bees that foraged on Asclepias incarnata (ASC) had four times as many pathogens, on average, than did bees that foraged on Digitalis purpurea (DIG) (top graph below). Bees foraging on Asclepias were much more likely to get infected (had greater susceptibility) than bees that foraged on several other species, most notably Linaria vulgaris (LIN) and Eupatorium perfoliatum (EUP) (middle graph). Lastly, if we limit our consideration to infected bees, the mean intensity of the infection was much greater for bees foraging on some species, such as Asclepias and Monarda didyma (MON) than on others, such as Digitalis and Antirrhinum majus (ANT) (bottom graph).

(Top graph) Mean number of Crithidia (2 microliter gut sample) hosted by bees after foraging on one of 14 different flowering plant species. This graph includes both infected and uninfected bees. (Middle graph) Susceptibility – the proportion of bees infected – after foraging trials on different plant species. (Bottom graph) Intensity of infection – Mean number of Crithidia for infected bees only. The capital letters below the graph are the first three letters of the plant genus. Numbers in bars are sample size. Error bars indicate 1 standard error.

It would be impossible to repeat this experiment on the 369,000 known species of flowering plants (with many more still to be identified). So Adler and her colleagues really wanted to know whether there were some flower characteristics or traits associated with plant species that served as the best vectors of disease. The researchers measured and counted variables associated with the flowers, such as the size and shape of the corolla, the number of open flowers and the number of reproductive structures (flowers, flower buds and fruits) per inflorescence.

Flower traits measured by Adler and colleagues (example for blue lobelia, Lobelia siphilitica). CL is corolla length. CW is corolla width. PL is petal length. PW is petal width. Credit: Melissa Ha.

The researchers also wanted to know whether any variables associated with the bees, such as bee size and bee behavior, would predict how likely it was that a bee would get infected. Surprisingly, the number of reproductive structures per inflorescence stood out as the most important variable. In addition, smaller bees were somewhat more likely to get infected than larger bees, and bees that foraged for a longer time period were more prone to infection.

Mean susceptibility of bees to Crithidia infection after foraging on 14 different flowering plant species, in relation to the number of reproductive structures (flowers, buds and fruits) per inflorescence.

These findings are both surprising and exciting. Adler and her colleagues were surprised to find such big differences in the ability of plant species to transmit disease. In addition, they were puzzled about the importance of number of reproductive structures per inflorescence. At this point, they don’t have a favorite hypothesis for its overriding importance, speculating that some unmeasured aspect of floral architecture influencing disease transmission might be related to the number of reproductive structures per inflorescence.

Bumblebee forages on Penstemon digitalis. In addition to the open flowers, note the large number of unopened buds. Each of these counted as a reproductive structure for the graph above. Credit: Jonathan Giacomini.

The world is losing pollinators at a rapid rate, and there are concerns that if present trends continue, there may not be enough pollinators to pollinate flowers of some of our most important food crops. Disease is implicated in many of these declines, so it behooves us to understand how plants can serve as vectors of diseases that affect pollinators. Identifying floral traits that influence disease transmission could guide the creation of pollinator-friendly habitats within plant communities, and help to maintain diverse pollinator communities within the world’s ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Adler, L. S., Michaud, K. M., Ellner, S. P., McArt, S. H., Stevenson, P. C. and Irwin, R. E. (2018), Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees. Ecology, 99: 2535-2545. doi:10.1002/ecy.2503. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Dinoflagellates deter copepod consumption

February 18, 2019 by fredsingerecology

Those of us who enjoy eating seafood are dismayed by the dreaded red tide, which renders some of our favorite prey toxic to us. A red tide occurs when dinoflagellates and other algae increase sharply in abundance, often in response to upwelling of nutrients from the ocean floor. Many of these dinoflagellates are red or brownish-red in color, so large numbers of them floating on or near the surface give the ocean its characteristic red color. These dinoflagellates produce toxic compounds (in particular neurotoxins) that pass through the food web, ultimately contaminating fish, molluscs and many other groups of species.

Red tide at Isahaya Bay, Japan. Credit: Marufish/Flickr.

Did toxicity arise in dinoflagellates to protect them from being eaten by predators – in particular by voracious copepods? The problem with this hypothesis is that copepods eat an entire dinoflagellate. Let’s imagine a dinoflagellate with a mutation that produces a toxic substance. At some point the dinoflagellate gets eaten, and the poor copepod consumer is exposed to the toxin. Maybe it dies and maybe it lives, but the important result is that the dinoflagellate dies, and its mutant genes are gone forever, along with the toxic trait. The only way toxicity will benefit the dinoflagellate individual, and thus spread throughout the dinoflagellate population, is if it increases the survival/reproductive success of individuals with the toxic trait. This can occur if copepods have some mechanism for detecting toxic dinoflagellates, and are therefore less likely to eat them.

Jiayi Xu and Thomas Kiørboe went looking for such a mechanism using 13 different species or strains of dinoflagellates that were presented to the copepod Temora longicornis. This copepod beats its legs to create an ocean current that moves water, and presumably dinoflagellates, in its direction, which it then eats. For their experiment, the researchers glued a hair to the dorsal surface of an individual copepod (very carefully), and they then attached the other side of the hair to a capillary tube, which was controlled by a micromanipulator. They placed these copepods into small aquaria, where the copepods continued to beat their legs, eat and engage in other bodily functions.

Aquarium with tethered copepod and recording equipment: Credit: J. Xu.

The researchers then added a measured amount of one type of dinoflagellate into the aquarium, and using high resolution videography, watched the copepods feed over the next 24 hours.

Tethered copepod beats its legs to attract a dinoflagellate (round blue circular cell). Credit: J. Xu.

Twelve of the dinoflegellate strains were known to be toxic, though they had several different types of poison. Protoceratium reticulatum was a nontoxic control species of dinoflagellate. As you can see below, on average, copepods ate more of the nontoxic P. reticulatum than they did of any of the toxic species.

Average dinoflagellate biomass ingested by the tethered copepods. P. reticulatum is the nontoxic control. Error bars are 1 SE.

Xu and Kiørboe identified two major mechanisms that underlie selectivity by the copepod predator. In many cases, the copepod successfully captured the prey, but then rejected it (top graph below). For one strain of A. tamarense prey, and a lesser extent for K. brevis prey, the predator simply fed less as a consequence of reducing the proportion of time that it beat its feeding legs (bottom graph below).

Copepod feeding behavior on 13 dinoflagellate prey species. Top graph is fraction of dinoflagellates rejected, while bottom graph is the proportion of time the copepods beats its feeding legs in the presence of a particular species/strain of dinoflagellate.

If you look at the very first graph in this post, which shows the average dinoflagellate biomass consumed, you will note that both strains of K. brevis (K8 and K9) are eaten very sparingly. The graphs just above show that the copepod rejects some K. brevis that it captures, and beats its legs a bit less often when presented with K. brevis. However, the rejection increase and leg beating decreases are not sufficient to account for the tremendous reduction in consumption. So something else must be going on. The researchers suspect that the copepod can identify K. breviscells from a distance, presumably through olfaction, and decide not to capture them. This mechanism warrants further exploration.

One surprising finding of this study is that the copepod responds differently to one strain of the same species (A. tamarense) than it does to the other strains. Xu and Kiorbe point out that previous studies of copepod/dinoflagellate interactions have identified other surprises. For example, there are cases where a dinoflagellate strain is toxic to one strain of copepod, but harmless to another copepod strain of the same species. Also, within a dinoflagellate species, one strain may have a very different distribution of toxins than does a second strain. So why does this degree of variation exist in this system?

The researchers argue that there may be an evolutionary arms race between copepods and dinoflagellates. The copepod adapts to the toxin of co-occurring dinoflagellates, becoming resistant to the toxin. This selects for dinoflagellates that produce a novel toxin that the copepod is sensitive to. Over time, the copepod evolves resistance to the second toxin as well, and so on… Because masses of ocean water and populations of both groups are constantly mixing, different species and strains are exposed to novel environments with high frequency. Evolution happens.

note: the paper that describes this research is from the journal Ecology. The reference is Xu, J. and Kiørboe, T. (2018), Toxic dinoflagellates produce true grazer deterrents. Ecology, 99: 2240-2249. doi:10.1002/ecy.2479. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Decomposition: it’s who you are and where you are

February 11, 2019 by fredsingerecology

“Follow the carbon” is a growing pastime of ecologists and environmental researchers worldwide. In the process of cellular respiration, organisms use carbon compounds to fuel their metabolic pathways, so having carbon around makes life possible. Within ecosystems, following the carbon is equivalent to following how energy flows among the producers, consumers, detritivores and decomposers. In soils, decomposers play a central role in energy flow, but we might not appreciate their importance because many decomposers are tiny, and decomposition is very slow. We are thrilled by a hawk subduing a rodent, but are less appreciative of a bacterium breaking down a lignin molecule, even though at their molecular heart, both processes are the same, in that complex carbon enters the organism and fuels cellular respiration. However. from a global perspective, cellular respiration produces carbon dioxide as a waste product, which if allowed to escape the ecosystem, will increase the pool of atmospheric carbon dioxide thereby increasing the rate of global warming. So following the carbon is an ecological imperative.

As the world warms, trees and shrubs are colonizing regions that previously were inaccessible to them. In northern Sweden, mountain birch forests (Betula pubescens) and birch shrubs (Betula nana) are advancing into the tundra, replacing the heath that is dominated by the crowberry, Empetrum nigrum. As he began his PhD studies, Thomas Parker became interested in the general question of how decomposition changes as trees and shrubs expand further north in the Arctic. On his first trip to a field site in northern Sweden he noticed that the areas of forest and shrubs produced a lot of leaf litter in autumn yet there was no significant accumulation of this litter the following year. He wondered how the litter decomposed, and how this process might change as birch overtook the crowberry.

One of the study sides in autumn: mountain birch forest (yellow) in the background, dwarf birch (red) on the left and crowberry on the right. Credit: Tom Parker.

Several factors can affect leaf litter decomposition in northern climes. First, depending on what they are made of, different species of leaves will decompose at different rates. Second, different types of microorganisms present will target different types of leaves with varying degrees of efficiency. Lastly, the abiotic environment may play a role; for example, due to shade and creation of discrete microenvironments, forests have deeper snowpack, keeping soils warmer in winter and potentially elevating decomposer cellular respiration rates. Working with several other researchers, Parker tested the following three hypotheses: (1) litter from the more productive vegetation types will decompose more quickly, (2) all types of litter decompose more quickly in forest and shrub environments, and (3) deep winter snow (in forest and shrub environments) increase litter decomposition compared to heath environments.

To test these hypotheses, Parker and his colleagues established 12 transects that transitioned from forest to shrub to heath. Along each transect, they set up three 2 m² plots – one each in the forest, shrub, and heath – 36 plots in all. In September of 2012, the researchers collected fresh leaf littler from mountain birch, shrub birch and crowberry, which they sorted, dried and placed into 7X7 cm. polyester mesh bags. They placed six litter bags of each species at each of the 36 plots, and then harvested these bags periodically over the next three years. Bags were securely attached to the ground so that small decomposers could get in, but the researchers had to choose a relatively small mesh diameter to make sure they successfully enclosed the tiny crowberry leaves. This restricted access to some of the larger decomposers.

Some litter bags attached to the soil surface at the beginning of the experiment. Credit: Tom Parker.

To test for the effect of snow depth, the researchers also set up snow fences on nearby heath sites. These fences accumulated blowing and drifting snow, creating a snowpack comparable to that in nearby forest and shrub plots.

Parker and his colleagues found that B. pubescens leaves decomposed most rapidly and E. nigrum leases decomposed most slowly. In addition, leaf litter decomposed fastest in the forest and most slowly in the heath. Lastly, snow depth did not influence decomposition rate.

(Left graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath, shrub and forest. (Right graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars are 1 SE.

B. pubescens in forest and shrub lost the greatest amount (almost 50%) of mass over the three years of the study, while E. nigrum in heath lost the least (less than 30%). However, B. pubescens decomposed much more rapidly in the forest than in the shrub between days 365 and 641. The bottom graphs below show that snow fences had no significant effect on decomposition.

Percentage of litter mass remaining (a, d) E. nigrum, (b, e) B. nana, (c, f) B. pubescens in heath, shrub, or forest. Top graphs (a, b, c) are natural transects, while the bottom graphs (d, e, f) represent heath tundra under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars represent are 1SE. Shaded areas on the x-axis indicate the snow covered season in the first two years of the study.

Why do mountain birch leaves decompose so much more than do crowberry leaves? The researchers chemically analyzed both species and discovered that birch leaves had 1.7 times more carbohydrate than did crowberry, while crowberry had 4.9 times more lipids than did birch. Their chemical analysis showed much of birch’s rapid early decomposition was a result of rapid carbohydrate breakdown. In contrast, crowberry’s slow decomposition resulted from its high lipid content being relatively resistant to the actions of decomposers.

Researchers (Parker right, Subke left) harvesting soils and litter in the tundra. Credit: Jens-Arne Subke.

Parker and his colleagues did discover that decomposition was fastest in the forest independent of litter type. Forest soils are rich in brown-rot fungi, which are known to target the carbohydrates (primarily cellulose) that are so abundant in mountain birch leaves. The researchers propose that a history of high cellulose litter content has selected for a biochemical environment that efficiently breaks down cellulose-rich leaves. Once the brown-rot fungi and their allies have done much of the initial breakdown, another class of fungi (ectomycorrhizal fungi) kicks into action and metabolizes (and decomposes) the more complex organic molecules.

The result of all this decomposition in the forest, but not the heath, is that tundra heath stores much more organic compounds than does the adjacent forest (which loses stored organic compounds to decomposers). As forests continue their relentless march northward replacing the heath, it is very likely that they will introduce their efficient army of decomposers to the former heathlands. These decomposers will feast on the vast supply of stored organic carbon compounds, release large quantities of carbon dioxide into the atmosphere, which will further exacerbate global warming. This is one of several positive feedbacks loops expected to destabilize global climate systems in the coming years.

note: the paper that describes this research is from the journal Ecology. The reference is Parker, T. C., Sanderman, J., Holden, R. D., Blume‐Werry, G., Sjögersten, S., Large, D., Castro‐Díaz, M., Street, L. E., Subke, J. and Wookey, P. A. (2018), Exploring drivers of litter decomposition in a greening Arctic: results from a transplant experiment across a treeline. Ecology, 99: 2284-2294. doi:10.1002/ecy.2442. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Rice fields foster biodiversity

January 11, 2019 by fredsingerecology

Restoration ecologists want to restore ecosystems that have been damaged or destroyed by human activity. One approach they use is “rewilding” – which can mean different things to different people. To some, rewilding involves returning large predators to an ecosystem, thereby reestablishing important ecological linkages. To others, rewilding requires corridors that link different wild areas, so animals can migrate from one area to another. One common thread in most concepts of rewilding is that once established, restored ecosystems should be self-sustaining, so that if ecosystems are left to their own devices, ecological linkages and biological diversity can return to pre-human-intervention levels, and remain at those levels in the future.

ardea intermedia (intermediate egret). photo by n. katayama

The intermediate egrit, Ardea intermedia, plucks a fish from a flooded rice field. Credit: N. Katayama.

Chieko Koshida and Naoki Katayama argue that rewilding may not always increase biological diversity. In some cases, allowing ecosystems to return to their pre-human-intervention state can actually cause biological diversity to decline. Koshida and Katayama were surveying bird diversity in abandoned rice fields, and noticed that bird species distributions were different in long-abandoned rice fields in comparison to still-functioning rice fields. To follow up on their observations, they surveyed the literature, and found 172 studies that addressed how rice field abandonment in Japan affected species richness (number of species) or abundance. For the meta-analysis we will be discussing today, an eligible study needed to compare richness and/or abundance for at least two of three management states: (1) cultivated (tilled, flood irrigated, rice planted, and harvested every year), (2) fallow (tilled or mowed once every 1-3 years), and (3) long-abandoned (unmanaged for at least three years).

Three different rice field management states – cultivated, fallow and long-abandoned – showing differences in vegetation and water conditions. Credit: C. Koshida.

Meta-analyses are always challenging, because the data are collected by many researchers, and for a variety of purposes. For example, some researchers may only be interested in whether invasive species were present, or they may not be interested in how many individuals of a particular species were present. Ultimately 35 studies met Koshida and Katayama’s criteria for their meta-analysis (29 in Japanese and six in English).

Overall, abandoning or fallowing rice fields decreased species richness or abundance to 72% of the value of cultivated rice fields. As you might suspect, these effects were not uniform for different variables or comparisons. Not surprisingly, fish and amphibians declined sharply in abandoned rice fields – much more than other groups of organisms. Abundance declined more sharply in abandoned fields than did species richness. Several other trends also emerged. For example, complex landscapes such as yatsuda (forested valleys) and tanada (hilly terraces) were more affected than were simple landscapes. In addition, wetter abandoned fields were able to maintain biological diversity, while dryer abandoned fields declined in richness and abundance.

The effects of rice field abandonment or fallowing for eight different variables. Effect size is the ln (Mt/Mc), where Mt = mean species richness or abundance for the treatment, and Mc = mean species richness for the control. The treated field in all comparisons was the one that was abandoned for the longer time. A positive effect size means that species richness or abundance increased in the treated (longer abandoned) field, while a negative effect size means that species richness or abundance declined in the treated field. Numbers in parentheses are number of data sets used for comparisons.

When numerous variables are considered, researchers need to figure out which are most important. Koshida and Katayama used a statistical approach known as “random forest” to model the impact of different variables on the reduction in biological diversity following abandonment. This approach generates a variable – the percentage increase in mean square error (%increaseMSE) – which indicates the importance of each variable for the model (we won’t go into how this is done!). As the graph below shows, soil moisture was the most important variable, which tells us (along with the previous figure above) that abandoned fields that maintained high moisture levels also kept their biological diversity, while those that dried out lost out considerably. Management state was the second most important variable, as long-abandoned fields lost considerably more biological diversity than did fallow fields.

Importance estimates of each variable (as measured by %increase MSE). Higher values indicate greater importance.

Unfortunately, only three studies had data on changes in biological diversity over the long-term. All three of these studies surveyed plant species richness over a 6 – 15 year period, so Koshida and Katayama combined them to explore whether plant species richness recovers following long-term rice field abandonment. Based on these studies, species richness continues to decline over the entire time period.

Plant species richness in relation to time since rice fields were abandoned (based on three studies).

Koshida and Katayama conclude that left to their own devices, some ecosystems, like rice fields, will actually decrease, rather than increase, in biological diversity. Rice fields are, however, special cases, because they provide alternatives to natural wetlands for many organisms dependent on aquatic/wetland environments (such as the frog below). In this sense, rice fields should be viewed as ecological refuges for these groups of organisms.

rana-porosa-porosa-tokyo-daruma-pond-frog.-photo-by-y.g.-baba.jpg

Rana porosa porosa (Tokyo Daruma Pond Frog). Credit: Y. G. Baba

These findings also have important management implications. For example, conservation ecologists can promote biological diversity in abandoned rice fields by mowing and flooding. In addition, managers should pay particular attention to abandoned rice fields with complex structure, as they are particularly good reservoirs of biological diversity, and are likely to lose species if allowed to dry out. Failure to attend to these issues could lead to local extinctions of specialist wetland species and of terrestrial species that live in grasslands surrounding rice fields. Lastly, restoration ecologists working on other types of ecosystems need to carefully consider the effects on biological diversity of allowing those ecosystems to return to their natural state without any human intervention.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Koshida, C. and Katayama, N. (2018), Meta‐analysis of the effects of rice‐field abandonment on biodiversity in Japan. Conservation Biology, 32: 1392-1402. doi:10.1111/cobi.13156. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

Sweltering ants seek salt

December 30, 2018 by fredsingerecology

Like humans, ants need salt and sugar. Salt is critical for a functioning nervous system and for maintaining muscle activity, while sugar is a ready energy source. In ectotherms such as ants, body temperature is influenced primarily by the external environment, with higher environmental temperatures leading to higher body temperatures. When ants get hot their metabolic rates rise, so they can go out and do energetically demanding activities such as foraging for essential resources like salt and sugar. On the down side, hot ants excrete more salt and burn up more sugar. In addition, like humans, very high body temperature can be lethal, so ants are forced to seek shelter during extreme heat. As a beginning graduate student, Rebecca Prather wanted to know whether ants adjust their foraging rates on salt and sugar in response to the conflicting demands of elevated temperatures on ants’ physiological systems.

Rebecca Prather at her field site in Oklahoma, USA. Credit: Rebecca Prather.

Prather and her colleagues studied two different field sites: Centennial Prairie is home to 16 ant species, while Pigtail Alley Prairie has nine species. For their first experiment, the researchers established three transects with 100 stations baited with vials containing cotton balls and either 0.5% salt (NaCl) or 1% sucrose. The bait stations were 1 meter apart. After 1 hour, they collected the vials (with or without ants), and counted and identified each ant in each vial. The researchers measured soil temperature at the surface and at a depth of 10 cm. The researchers repeated these experiments at 9 AM, 1 PM and 5 PM, April – October, 4 times each month.

Ants recruited to vials with 0.5% salt solution. Credit: Rebecca Prather.

Sugar is easily stored in the body, so while sugar consumption increases with temperature, due to increased ant metabolic rate, sugar excretion is relatively stable with temperature. In contrast, salt cannot be stored effectively, so salt excretion increases at high body temperature. Consequently, Prather and her colleagues expected that ant salt-demand would increase with temperature more rapidly than would ant sugar-demand.

Ant behavior in response to vials with 0.5% salt (dark circles) and 1% sucrose (white circles) at varying soil temperatures at 9AM, 1 PM (13:00) and 5PM (17:00). The three left graphs show the number of vials discovered (containing at least one ant), while the three right graphs show the number of ants recruited per vial. The Q10 value = the rate of discovery or recruitment at 30 deg. C divided by the rate of discovery or recruitment at 20 deg. C. * indicates that the two curves have statistically significantly different slopes.

The researchers discovered that ants foraged more at high temperatures. However, when surface temperatures were too high (most commonly at 1 PM during summer months), ants could not forage and remained in their nests. At all three times of day, ants discovered more salt vials at higher soil temperatures. Ants also discovered more sugar vials at higher temperatures in the morning and evening, but not during the 1 PM surveys. Most interesting, the slope of the curve was much steeper for salt discovery than it was for sugar discovery, indicating that higher temperature increased salt discovery rate more than it increased sugar discovery rate (three graphs on left).

When ants discover a high quality resource, they will recruit other nestmates to the resource to help with the harvest. Ant recruitment rates increased with temperature to salt, but not sugar, indicating that ant demand for 0.5% salt increased more rapidly than ant demand for 1% sugar (three graphs above on right).

The researchers were concerned that the sugar concentrations were too low to excite much recruitment, so they replicated the experiments the following year using four different sugar concentrations. Ant recruitment was substantially greater to higher sugar concentrations, but was still two to three times lower than it was to 0.5% salt.

Ant recruitment (y-axis) to different sugar concentrations at a range of soil temperatures (X-axis). Q10 values are to the left of each line of best fit.

Three of the four most common ant species showed the salt and sugar preferences that we described above, but the other common species, Formica pallidefulva, actually decreased foraging at higher temperatures. The researchers suggest that this species is outcompeted by the other more dominant species at high temperatures, and are forced to forage at lower temperatures when fewer competitors are present.

In a warming world, ant performance will increase as temperatures increase up to ants’ thermal maximum, at which point ant performance will crash. Ants are critical to ecosystems, playing important roles as consumers and as seed dispersers. Thus many ecosystems in which ants are common (and there are many such ecosystems!) may function more or less efficiently depending on how changing temperatures influence ants’ abilities to consume and conserve essential nutrients such as salt.

note: the paper that describes this research is from the journal Ecology. The reference is Prather, R. M., Roeder, K. A., Sanders, N. J. and Kaspari, M. (2018), Using metabolic and thermal ecology to predict temperature dependent ecosystem activity: a test with prairie ants. Ecology, 99: 2113-2121. doi:10.1002/ecy.2445 . Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

What grows up must go down: plant species richness and soils below.

November 29, 2018 by fredsingerecology

Almost 20 years ago, Dorota Porazinska was a postdoctoral researcher investigating whether plant diversity influenced the diversity of organisms that lived in the soil below these plants, including bacteria, protists, fungi and nematodes (collectively known as soil biota). Surprisingly, she and her colleagues discovered no linkages between aboveground and belowground species diversity. She suspected that two issues were responsible for this lack of linkage. First, the early study lumped related species into functional groups – for example nematodes that eat bacteria, or nematodes that eat fungi. Lumping simplifies data collection but loses a lot of data because individual species are not distinguished. Back in those days, identifying species with DNA analysis was time-consuming, expensive, and often impractical. The second issue was that even if aboveground-belowground diversity was linked, it might be difficult to detect. Ecosystems are very complex, and many belowground species make a living off of legacies of carbon or other nutrients that are the remains of organisms that lived many generations ago. These legacy organic nutrient pools allow for indirect (and thus more difficult to detect) linkages between aboveground and belowground species.

Porazinska and her colleagues reasoned that if there were aboveground/belowground relationships, they would be easiest to detect in the simplest ecosystems that lacked significant pools of legacy nutrients. They also used molecular techniques that were not readily available for earlier studies to identify distinct species based on DNA analysis. The researchers established 98 1-m radius circular plots at the Niwot Ridge Long Term Ecological Research Site in the Colorado, USA Rocky Mountains. At each plot, they identified and counted each vascular plant, and recorded the presence of moss and lichen. They also censused soil biota by using a variety of DNA amplification and isolation techniques that allowed them to identify bacteria, archaea, protists, fungi and nematodes to species.

Field assistant Jarred Huxley surveys plants in a high species richness plot. Credit Dorota L. Porazinska.

As expected in this alpine environment, plant species richness was quite low, averaging only 8 species per plot (range = 0 – 27). In contrast to what had been found in other ecosystems, high plant diversity was associated with high diversity of soil biota.

Relationship between plant richness (x-axis) and soil biota richness (y-axis) for (A) bacteria, (B) eukaryotes (excluding fungi and nematodes), (C) fungi, and (D) nematodes. OTUs are operational taxonomic units, which represent organisms with very similar or identical DNA sequences on a marker gene. For our purposes, they represent distinct species.

Looking at the graphs above, you can see that different groups responded to different degrees; nematodes had the strongest response to increases in plant richness while fungi had the weakest response. When viewed at a finer level, some groups of soil organisms, including photosynthetic microorganisms such as cyanobacteria and green algae actually decreased, presumably in response to competition with aboveground plants for light and possibly nutrients.

Given the strong relationship between plant species richness and soil biota richness, Porazinska and her colleagues next explored whether high plant richness was associated with soil nutrient levels (nutrient pools). In general, there was a strong correlation between plant species richness and nutrient pools (see graphs below). But soil moisture, and the ability of soil to hold moisture were the two most important factors associated with nutrient pools.

Amount (micrograms per gram of soil) of carbon (left graph) and nitrogen (right graph) in relation to plant species richness.

Ecologists studying soil processes can measure the rates at which microorganisms are metabolizing nutrients such as carbon, phosphorus and nitrogen. The expectation was that if high plant species richness was associated with higher soil biota richness, and larger soil nutrient pools, then the activity of enzymes that metabolize soil nutrients should proportionally increase with these factors. The researchers found that enzyme activity was very low where plants were absent or rare, and greatest in complex plant communities. But the most important factors influencing enzyme activity were the amount of organic carbon present within the soil, and the ability of the soil to hold water.

Patchy vegetation at the field site. Credit: Cliffton P. Bueno de Mesquita.

Porazinska and her colleagues hypothesize that the relationship between plant species richness, soil biota richness, nutrient pools, and soil processes such as enzyme activity, exist in most ecosystems, but are obscured by indirect linkages between these different levels. They hypothesize that these relationships in other ecosystems such as grasslands and forests are difficult to observe. In these more complex ecosystems, carbon inputs into the soil form large legacy carbon pools. These carbon pools, and the ability of the soil to hold nutrient pools, fundamentally influence the abundance and richness of soil biota. In contrast, in nutrient-poor soils, such as high Rocky Mountain alpine meadows, legacy carbon pools are rare and small. Consequently, plants and soil biota interact more directly, and correlations between plant species diversity and soil biota diversity are much easier to detect.

note: the paper that describes this research is from the journal Ecology. The reference is Porazinska, D. L., Farrer, E. C., Spasojevic, M. J., Bueno de Mesquita, C. P., Sartwell, S. A., Smith, J. G., White, C. T., King, A. J., Suding, K. N. and Schmidt, S. K. (2018), Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology, 99: 1942-1952. doi:10.1002/ecy.2420. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

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